Frontline: Interferon regulatory factor-1 as a protective gene in intestinal inflammation: Role of TCR γ δ T cells and interleukin-18-binding protein

European Journal of Immunology

Volumn 34, Issue 9, 2004, Pages 2356-2364

  Siegmund, Britta ^a,d   Sennello, Joseph A ^a   Lehr, Hans A ^b   Senaldi, Giorgio ^c,e   Dinarello, Charles A ^a   Fantuzzi, Giamila ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c AMGEN INC   (United States)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e Abgenix Inc   (United States)

Author keywords

T cells; IL 18BP; Intestinal inflammation; IRF 1

Indexed keywords

CYCLOOXYGENASE 2; DEXTRAN SULFATE; GAMMA INTERFERON ANTIBODY; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 18 BINDING PROTEIN; INTERLEUKIN 1BETA; NEUTRALIZING ANTIBODY; STAT3 PROTEIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA; DNA BINDING PROTEIN; GAMMA INTERFERON; GLYCOPROTEIN; INTERLEUKIN-18 BINDING PROTEIN; IRF1 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; PHOSPHOPROTEIN; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLON; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; ENTERITIS; FEMALE; GENE FUNCTION; HISTOLOGY; KNOCKOUT MOUSE; LETHALITY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SCORING SYSTEM; T LYMPHOCYTE SUBPOPULATION; WILD TYPE; ANIMAL; C57BL MOUSE; COLITIS; GENETICS; MOUSE MUTANT; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; COLITIS; DNA-BINDING PROTEINS; FEMALE; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERFERON REGULATORY FACTOR-1; INTERFERON TYPE II; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOPROTEINS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 4644366900     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425124     Document Type: Article

References (44)

1. Fujita, T., Kimura, Y., Miyamoto, M., Barsoumian, E. L. and Taniguchi, T., Induction of endogenous IFN-α and IFN-β genes by a regulatory transcription factor, IRF-1. Nature 1989. 337: 270-278.
2. Galon, J., Sudarshan, C., Ito, S., Finbloom, D. and O'Shea, J. J., IL-12 induces IFN regulating factor-1 (IRF-1) gene expression in human NK and T cells. J. Immunol. 1999. 162: 7256-7261.
3. Harada, H., Fujita, T., Miyamoto, M., Kimura, Y., Maruyama, M., Furia, A., Miyata, T. and Taniguchi, T., Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 1989. 4: 729-734.
4. Miyamoto, M., Fujita, T., Kimura, Y., Maruyama, M., Harada, H., Sudo, Y., Miyata, T. and Taniguchi, T., Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-β gene regulatory elements. Cell 1988. 54: 903-909.
5. Lohoff, M., Ferrick, D., Mittrucker, H.-W., Duncan, G. S., Bischof, S., Rollinghoff, M. and Mak, T. W., Interferon regulator factor-1 is required for a T helper 1 immune response in vivo. Immunity 1997. 6: 681-689.
6. Tada, Y., Ho, A., Matsuyama, T. and Mak, T. W., Reduced incidence and severity of antigen-induced autoimmune diseases in mice lacking interferon regulatory factor-1. J. Exp. Med. 1997. 185: 231-238.
7. Fuss, I. J., Neurath, M., Boirivant, M., Klein, J. S., de la Motte, C., Strong, S. A., Fiocchi, C. and Strober, W., Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-γ, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 1996. 157: 1261-1270.
8. Plevy, S. E., Landers, C. J., Prehn, J., Carramanzana, N. M., Deem, R. L., Shealy, D. and Targan, S. R., A role for TNF-α and mucosal T helper-1 cytokines in the pathogenesis of Crohn's disease. J. Immunol. 1997. 159: 6276-6282.
9. Kelley, T. J. and Elmer, H. L., In vivo alterations of IFN regulatory factor-1 and PIAS1 protein levels in cystic fibrosis epithelium. J. Clin. Invest. 2000. 106: 403-410.
10. Ohteki, T., Yoshida, H., Matsuyama, T., Duncan, G. S., Mak, T. W. and Ohashi, P. S., The transcription factor interferon regulatory factor 1 (IRF-1) is important during the maturation of natural killer 1.1+ T cell receptor-α/β+ (NK1+ T) cells, natural killer cells, and intestinal intraepithelial T cells. J. Exp. Med. 1998. 187: 967-972.
11. Penninger, J. M., Sirard, C., Mittrucker, H. W., Chidgey, A., Kozieradzki, I., Nghiem, M., Hakem, A., Kimura, T., Timms, E., Boyd, R. et al., The interferon regulatory transcription factor IRF-1 controls positive and negative selection of CD8+ thymocytes. Immunity 1997. 7: 243-254.
12. Taki, S., Sato, T., Ogasawara, K., Kukuda, T., Sato, M., Hida, S., Suzuki, G., Mitsuyama, M., Shin, E. H., Kojima, S. et al., Multistage regulation of Th1-type immune responses by the transcription factor IRF-1. Immunity 1997. 6: 673-680.
13. Fantuzzi, G., Reed, D. A., Qi, M., Dinarello, C. A. and Senaldi, G., Role of interferon regulatory factor-1 in the regulation of IL-18 production and activity. Eur. J. Immunol. 2001. 31: 369-375.
14. Hurgin, V., Novick, D. and Rubinstein, M., The promoter of IL-18 binding protein; activation byan IFN-γ-induced complex of IFN regulatory factor 1 and CCAT/enhancer binding protein β. Proc. Nat. Acad. Sci. USA 2002. 99: 16957-16962.
15. Liu, J., Cao, S., Herman, L. M. and Ma, X., Differential regulation of interleukin (IL)-12 p35 and p40 gene expression and interferon (IFN)-γ primed IL-12 production by IFN regulatory factor 1. J. Exp. Med. 2003. 198: 1265-1276.
16. Ogasawara, K., Hida, S., Azimi, N., Tagaya, Y., Sato, T., Yokochi-Fukuda, T., Waldmann, T. A., Taniguchi, T. and Taki, S., Requirement for IRF-1 in the microenvironment supporting development of natural killer cells. Nature 1998. 391: 700-703.
17. Okayasu, I., Hatakeyama, S., Yamada, M., Okhusa, T., Inagaki, Y. and Nakaya, R., A novel method for the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990. 98: 694-702.
18. Strober, W., Fuss, I. J. and Blumberg, R. S., The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002. 20: 495-549.
19. Siegmund, B., Lehr, H. A. and Fantuzzi, G., Leptin: a pivotal mediator of intestinal inflammation. Gastroenterology 2002. 122: 2011-2025.
20. Taniguchi, T., Ogasawara, K., Takaoka, A. and Tanaka, N., IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 2001. 19: 623-655.
21. Suzuki, A., Hanada, T., Mitsuyama, K., Yoshida, T., Kamizono, S., Hoshino, T., Kubo, M., Yamashita, A., Okabe, M., Takeda, K. et al., Cis3/socs3/ssi3 plays a negative regulatory role in stat3 activation and intestinal inflammation. J. Exp. Med. 2001. 193: 471-482.
22. Hans, W., Scholmerich, J., Gross, V. and Falk, W., Interleukin-12 induced interferon-γ increases inflammation in acute dextran sulfate sodium induced colitis in mice. Eur. Cytokine Netw. 2000. 11: 67-74.
23. Chen, Y., Chou, K., Fuchs, E., Havran, W. L. and Boismenu, R., Protection of the intestinal mucosa by intraepithelial γ δ T cells. Proc. Natl. Acad. Sci. U S A 2002. 99: 14338-14343.
24. Tsuchiya, T., Fukuda, S., Hamada, H., Nakamura, A., Kohama, Y., Ishikawa, H., Tsujikawa, K. and Yamamoto, H., Role of γ δ T cells in the inflammatory response of experimental colitis mice. J. Immunol. 2003. 171: 5507-5513.
25. Siegmund, B., Fantuzzi, G., Rieder, F., Gamboni-Robertson, F., Lehr, H. A., Hartmann, G., Dinarello, C. A., Endres, S. and Eigler, A., Neutralization of IL-18 reduces severity in murine colitis and intestinal IFN-γ and TNF-α production. Am. J. Physiol. 2001. 281: R1264-R1273.
26. Ten Hove, T., Corbaz, A., Amitai, H., Aloni, S., Belzer, I., Graber, P., Drillenburg, P., van Deventer, S. J., Chvatchko, Y. and Te Velde, A. A., Blockade of endogenous IL-18 ameliorates TNBS-induced colitis by decreasing local TNF-α production in mice. Gastroenterology 2001. 121: 1372-1379.
27. Sivakumar, P. V., Brown, S. N., Goldrath, A. W., van der Vuurst de Vries, A. R., Viney, J. L. and Kennedy, M. K., IL-15. Insights from characterizing IL-15-deficient mice. In Fantuzzi, G. (Ed.) Cytokine Knockouts, 2nd Edition. Humana Press, Totowa, NJ, USA 2003, pp 281-301.
28. Senaldi, G., Shaklee, C. L., Guo, J., Martin, L., Boone, T., Mak, T. W. and Ulich, T. R., Protection against the mortality associated with disease models mediated by TNF and IFN-γ in mice lacking IFN regulatory factor-1. J. Immunol. 1999. 163: 6820-6826.
29. Krieglstein, C. F., Cerwinka, W. H., Leroux, F. S., Salter, J. W., Russell, J. M., Schuermann, G., Grisham, M. B., Ross, C. R. and Granger, D. N., Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J. Exp. Med. 2001. 194: 1207-1218.
30. Morteau, O., Morham, S. G., Sellon, R. K., Dieleman, L. A., Langenbach, R., Smithies, O. and Sartor, S. B., Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cylooxygenase-2. J. Clin. Invest. 2000. 105: 469-478.
31. Blanco, J. C., Contursi, C., Salkowski, C. A., DeWitt, D. L., Ozato, K. and Vogel, S. N., Interferon regulatory factor (IRF)-1 and IRF-2 regulate interferon γ-dependent cyclooxygenase 2 expression. J. Exp. Med. 2000. 191: 2131-2144.
32. Ashkar, A. A., Black, G. P., Wei, Q., He, H., Liang, L., Head, J. R. and Croy, B. A., Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 2003. 171: 2937-2944.
33. Meijssen, M. A., Brandwein, S. L., Reinecker, H. C., Bhan, A. K. and Podolsky, D. K., Alteration of gene expression by intestinal epithelial cells precedes colitis in interleukin-2-deficient mice. Am. J. Physiol. 1998. 274: G472-G479.
34. Powrie, F., Leach, M. W., Mauze, S., Menon, S., Barcomb Caddle, L. and Coffman, R. L., Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ cells. Immunity 1994. 1: 553-562.
35. Camoglio, L., Te Velde, A. A., de Boer, A., ten Kate, F. J., Kopf, M. and van Deventer, S. J., Hapten-induced colitis associated with maintained Th1 and inflammatory responses in IFN-γ receptor-deficient mice. Eur. J. Immunol. 2000. 30: 1486-1495.
36. Mizoguchi, A., Mizoguchi, E. and Bhan, A. K., The critical role of interleukin-4 but not interferon γ in the pathogenesis of colitis in T-cell receptor α-mutant mice. Gastroenterology 1999. 116: 320-326.
37. Davidson, N. J., Hudak, S. A., Lesley, R. E., Menon, S., Leach, M. W. and Rennick, D. M., IL-12, but not IFNγ, plays a major role in sustaining the chronic phase of colitis in IL-10-deficient mice. J. Immunol. 1998. 161: 3143-3149.
38. Hoffmann, J. C., Peters, K., Henschke, S., Herrmann, B., Pfister, K., Westermann, J. and Zeitz, M., Role of T lymphocytes in rat 2,4,6-trinitrobenzene sulphonic acid (TNBS) induced colitis: increased mortality after γ δ T cell depletion and no effect of α β T cell depletion. Gut 2001. 48: 489-495.
39. Corbaz, A., ten Hove, T., Herren, S., Graber, P., Schwartsburd, B., Belzer, I., Harrison, J., Plitz, T., Kosco-Vilbois, M. H., Kim, S. H. et al., IL-18-binding protein expression by endothelial cells and macrophages is up-regulated during active Crohn's disease. J. Immunol. 2002. 168: 3608-3616.
40. Pizarro, T. T., Michie, M. H., Bentz, M., Woraratanadharm, J., Smith, M. F., Foley, E., Moskaluk, C. A., Bickston, S. J. and Cominelli, F., IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J. Immunol. 1999. 162: 6829-6835.
41. Wirtz, S., Becker, C., Blumberg, R. S., Galle, P. R. and Neurath, M., Treatment of T cell-dependent experimental colitis in SCID mice by local administration of an adenovirus expressing IL-18 antisense mRNA. J. Immunol. 2002. 168: 411-420.
42. Matsuyama, T., Kimura, T., Kitagawa, M., Pfeffer, K., Kawakami, T., Watanabe, N., Kundig, T. M., Amakawa, R., Kishihara, K., Wakeham, A. et al., Targeted disruption of IRF-1 and IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 1993. 75: 83-90.
43. Wieland, C. W., Siegmund, B., Senaldi, G., Vasil, M. L., Dinarello, C. A. and Fantuzzi, G., Pulmonary inflammation induced by Pseudomonas aeuriginosa lipopolysaccharide, phospholipase C and exotoxin A: role of interferon regulatory factor 1. Infect. Immun. 2002. 70: 1352-1358.
44. Fantuzzi, G., Reed, D. A. and Dinarello, C. A., Interleukin (IL)-12-induced interferon-γ is dependent on caspase-1 processing of the IL-18 precursor. J. Clin. Invest. 1999. 104: 761-767.